Effect of Forced Expirations on Mucus Clearance in Patients with Chronic Airflow Obstruction: Effect of Lung Recoil Pressure

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Thorax 1990;45:623-627 623 Effect of forced expirations on mucus clearance in patients with chronic airflow obstruction: effect of lung recoil pressure Thorax: first published as 10.1136/thx.45.8.623 on 1 August 1990. Downloaded from

C P van der Schans, D A Piers, H Beekhuis, G H Koeter, Th W van der Mark, D S Postma

Abstract spontaneous mucus clearance, the effect of Spontaneous mucus clearance and the forced expirations with an open glottis at effect of forced expirations and coughing different lung volumes, and the effect of on mucus clearance were investigated in coughing in patients with sputum production. eight patients with chronic airflow ob- We studied two groups of patients with struction and low elastic recoil pressure similar degrees of airways obstruction, one (emphysema group: mean FEVy 45% with normal elastic recoil pressure and the predicted) and in seven patients with other with decreased elastic recoil pressure. chronic airflow obstruction and normal For convenience we have labelled the two elastic recoil pressure (chronic bron- groups "chronic bronchitis" and chitis group: mean FEVy 57% predicted). "emphysema." Mucus clearance was measured in a central and a peripheral lung region by a radioactive aerosol tracer technique. Methods Spontaneous mucus clearance from the MUCUS CLEARANCE MEASUREMENTS peripheral lung region was higher in the Mucus transport in the lungs was measured as patients with emphysema than in those described elsewhere.9 In summary, a radio- with chronic bronchitis. There was no active aerosol was generated by means of an difference in central mucus clearance intermittent positive pressure respirator between the two groups. Mucus clear- (Bennet AP-5); the nebuliser was filled with ance from the peripheral lung region 35-50 MBq (1-15 mCi) technetium-99m increased significantly during forced labelled tin colloid (Amersham; 95% of the expirations and coughing in the patients particles 1-15 gum). In this way, a hetero-

with chronic bronchitis but not in those disperse aerosol is produced and 10-15% of http://thorax.bmj.com/ with emphysema. It is concluded that in the tracer would be deposited in the airways patients with chronic airflow obstruction after 40 inhalations. After inhaling the aerosol and regular sputum production sponta- patients were asked to wash their mouth and neous peripheral mucus clearance is drink water to clear their throat and oeso- greater in those with decreased elastic phagus of radioactive tracer. The initial whole recoil pressure. Physiotherapy that in- lung deposition pattern was quantified by cludes forced expirations and coughing expressing the amount of radioactive tracer in

can enhance mucus clearance in such the central and peripheral regions as percent- on September 24, 2021 by guest. Protected copyright. patients when elastic recoil pressure is ages of whole lung deposition. In each of the normal but is unlikely to be effective four studies the radiation dose to the lungs when elastic recoil pressure is decreased. with this method is 0-6 mGy (60 mrad) and the effective total body radiation dose 0.1 mGy (10 mrad).'° Division of Physiotherapy, Clearance measurements were made with Department of Physiotherapy is commonly used to treat the patient lying supine. A gamma camera was Rehabilitation mucus retention in patients with chronic air- positioned behind the thorax and linked to a C P van der Schans flow obstruction. These patients often have computer for continuous acquisition of one Department of increased mucus production in addition. Al- minute frames for 35 minutes. For data Nuclear Medicine D A Piers though retention of mucus is a complex analysis an oval central region was determined H Beekhuis problem and due to many different factors visually on the monitor. The size of this Department of physiotherapy is usually given. The forced region was recorded on the basis of the length Pulmonary Diseases expiration technique,l" in which a forced of the x and y axes. The peripheral region was G H Koeter expiration with an open glottis is carried out defined as the total lung region minus the Th W van der Mark D S Postma at different lung volumes, is commonly used central region (fig 1). Thus the sizes of the University Hospital, in an attempt to mobilise mucus by providing central and peripheral regions were indivi- Groningen, The a high expiratory axial airflow velocity in the dually reproducible over the four days of Netherlands airways.' measurement. The total amount of radioactive Address for reprint requests: We wondered whether forced expirations tracer in both lung regions was printed out C P van der Schans, Academisch Ziekenhuis, were less useful in patients with mucus pro- after correction for physical decay. The secr. Fysiotherapie CMC I, duction who have decreased elastic recoil results were expressed as percentages of the Oostersingel 59, 9713 EZ Groningen, The pressure than in patients with mucus produc- starting value, defined as the amount of Netherlands. tion and normal elastic recoil pressure. The radioactive tracer measured in the period 0-1 Accepted 2 April 1990 aim of the present study was to evaluate minute. The decrease of radioactive tracer was 624 van der Schans, Piers, Beekhuis, Koeter, van der Mark, Postma

Figure 1 Example ofa total lung region (a); the peripheral region (b) is found by subtracting the central region (c) from the

total lung region. Thorax: first published as 10.1136/thx.45.8.623 on 1 August 1990. Downloaded from

considered to reflect mucus transport in the Mucus clearance measurements were per- lungs. formed on each study day. The protocols were started after inhalation of the radiolabelled PATIENTS aerosol. After each protocol the patient was Eight patients were selected on the entry visit asked whether the treatment had been effec- on the basis of the following criteria and tive in clearing the lungs. None of the patients categorised as having emphysema: regular had used the forced expiration technique daily expectoration of mucus, airflow obstruc- previously. During each protocol the patients tion with an FEV, below 80% predicted and were required to lie supine for 35 minutes. values below predicted after bronchodilata- Protocols II, III, and IV were used in a tion, static pulmonary compliance above randomised order; protocol I was carried out 110% predicted, total lung capacity above on the first study day. The four protocols 110% predicted or FEV,/FIV, below 60%, were: and circumstantial evidence of emphysema on Protocol I This was used for control the chest radiograph according to the criteria measurements and for measuring spontaneous of Simon et al." Seven patients with chronic mucus clearance. No physiotherapy was per- bronchitis were also selected on an entry visit. formed. These patients had also regular daily expec- Protocol II The patients breathed undis- http://thorax.bmj.com/ toration of mucus, and an FEV1 below 80% turbed for the first 10 minutes. Forced expira- predicted that was not fully reversible. They tions with an open glottis were then perfor- had to have a static lung compliance med from total lung capacity (TLC) every 30 measurement below 90% predicted and had to seconds for a further 10 minutes. Patients show no clinical or radiological symptoms or then coughed as productively as possible signs suggesting emphysema. Spirometry was every 30 seconds for five minutes. The last 10 performed with a water sealed spirometer. minutes again consisted of undisturbed Static lung volumes were assessed with a

breathing. on September 24, 2021 by guest. Protected copyright. helium dilution technique. Pulmonary com- Protocol III This was the same as II except pliance was measured as outlined by Cotes."2 that the forced expirations were now perfor- Each patient with emphysema was matched as med at functional residual capacity (FRC). closely as possible for FEVy and smoking Protocol IV This consisted of 10 minutes of habits with a patient with chronic bronchitis. undisturbed breathing followed by a period of On the days of measurement the patients used coughing every 30 seconds for 15 minutes. their regular medication-that is, inhalation The patient then breathed again undisturbed steroids, ipratropium bromide, theophylline, for 10 minutes. and beta agonists. Routine physiotherapy was The patient took a drink of water to clear not performed on the days of measurement. the oesophagus of radioactive tracer after the The study was approved by the medical ethics forced expiration periods and after the cough- committee of the university hospital. All ing period. patients gave written, informed consent. PHYSIOTHERAPY Physiotherapy was always given by the same STATISTICAL ANALYSIS physiotherapist (C P vd S). The patients Differences in radioactive tracer clearance at underwent three different physiotherapy 10, 20, 25, and 35 minutes after starting the protocols (II, III, IV) and one protocol with- clearance measurements were compared without treatment (I) on four different days, in the two groups by means of analysis of always between 13.00 and 15.00 hours within variance. Differences between the two groups nine days. Peak expiratory flow (PEF) was were compared by means of Student's un- determined before each mucus clearance paired t test. In both tests a significant dif- measurement. The highest value from three ference was defined as p < 0 05. All calcu- technically correct manoeuvres was taken for lations were performed by using the SPSS analysis. statistical package.'3 Effect offorced expirations on mucus clearance in patients with chronic airflow obstruction: effect of lung recoil pressure 625

Table I Characteristics of the patients Mean Patient No: 1 2 3 4 5 6 7 8 (SD) Emphysema Thorax: first published as 10.1136/thx.45.8.623 on 1 August 1990. Downloaded from Age (y) 69 64 66 61 60 63 69 34 61 (11) FEV, (% pred) 44 35 72 66 45 33 38 30 45 (16) FEV, (% VC) 25 37 37 55 37 41 28 41 38 (9) FEV,/FIV, 33 38 60 58 44 46 31 30 43 (12) TLC(% pred) 129 140 120 115 120 95 137 130 123 (14) RV (%pred) 129 219 190 154 158 173 138 187 169 (30) C(%pred) 141 167 180 125 190 110 110 146 (33) Sputum(g)* 10(2) 19(3) 68(5) 4(1) 53(2) 12(3) 4(1) 13(2) 24 (24) Smokingt + + + + - + - - Medication S, I, B S, I, B, T I S, I, B S, I, B S, I S, I, B, T S, I, B, T Bronchitis Age (y) 62 65 51 72 70 43 64 61 (10) FEV, (% pred) 46 42 76 69 52 35 81 57 (18) FEV, (% VC) 54 32 55 70 46 36 65 51 (14)t FEVI/FIV, 44 45 63 68 50 48 84 57 (15)4 TLC(%pred) 150 90 113 66 96 109 100 103 (26)4 RV(%pred) 100 130 117 106 156 200 120 133 (35)4 C(%pred) 70 76 89 90 54 80 56 74 (15)4 Sputum(g)* 14(4) 56(17) 5(1) 32(3) 15(4) 4(2) 16(1) 20 (18)4 Smokingt + + + - + + - Medication S,I S,I,B,T S, I,T S,B S, I,B,T S,I S,I,T *Mean (SD) of the sputum production/day of three consecutive days. t + Indicates smoker and - non-smoker or ex-smoker. :Significant difference between patients with emphysema and those with bronchitis. S-inhalation corticosteroid; I-ipratropium bromide; T-theophylline; B-beta agonist; VC-slow inspiratory vital capacity; FEV,/FIV,-forced expiratory volume in one second as a percentage of the forced inspiratory volume in one second; TLC-total lung capacity; RV-residual volume; C-compliance.

Table 2 Mean (SD) peak expiratoryflow (I/min) before thefour different protocols Results The clinical Protocol I II III IV characteristics of both groups of patients at the beginning of the study are given Emphysema 238 (80) 263 (126) 258 (110) 237 (90) in table 1. There were no significant differences Bronchitis 251 (118) 250 (90) 249 (75) 281 (101) between the two groups for age, FEVy, or sputum production. FEV, % vital capacity

(VC) and FEV,/FIV1 were lower in the groups http://thorax.bmj.com/ with emphysema (p < 0-025, p < 0 05). TLC (% predicted), residual volume (RV; % predic- EMPHYSEMA ted) and compliance were higher in those with 14 emphysema (p < 0-05, p < 0 05, p < 0-0005). There was no significant difference in peak expiratory flow (PEF) values before the CD 12 measurements on the four study days in either of group patients (table 2). on September 24, 2021 by guest. Protected copyright. > 10 DEPOSITION OF TRACER In the patients with chronic bronchitis the CD) .~~------...... ~ ~~~~~~~~~~ mean _ 8 (SD) deposition of radioactive tracer in the central region on the four study days, n expressed as a percentage ofwhole lung , 6 deposi- 04 ...... tion, was 41 (4), 48 (11), 43 (8), and 45 (4); ...... CD ...... peripheral deposition (%) was 59 (4), 52 (11), ...... 57 (8), and 55 (4). In the patients with emphysema central deposition was 39 (17), 39 (12), 40 (14), and 40 (11); the peripheral ac deposition was 61 (17), 61 (12), 60 (14), and 60 0 ...... pr..... a -224 (11). The differences between the study days - ...... _...._._ and between the two groups were not n 0 significant.

r- MUCUS CLEARANCE Subjectively all patients thought that coughing was the only effective method of achieving mucus expectoration. -6 ...... _...... Emphysema There was no significant difference Figure 2 Clearance~~~~~~~~~...... of the radioactive tracer in the patients with emphysema from the in mucus peripheral lung region in the period 10-20 minutes during thefour different protocols, clearance in either the central or the peripheral expressed as a percentage of the starting value ~~~~~~~~~~~~~~~~~~.....(means and standard errors). lung region between the four protocols at any 626 van der Schans, Piers, Beekhuis, Koiter, van der Mark, Postma time (0-10, 10-20, 20-25, 25-35 minutes) (fig BRONCHITIS 2) or in the whole period (0-35 minutes). Chronic bronchitis There was no significant difference in peri- Thorax: first published as 10.1136/thx.45.8.623 on 1 August 1990. Downloaded from pheral mucus clearance between the four protocols in the period 0-10 minutes, when no physiotherapy was given. For the period 10-20 minutes peripheral mucus clearance during protocol I (control) was significantly lower than during the periods when forced expirations were performed at TLC (protocol II) or FRC (protocol III) or the patient was coughing (protocol IV) (p < 0 05) (fig 3). Central mucus clearance during this period did not differ significantly between the four protocols. There were no significant differences in peripheral mucus clearance in the periods 20-25 minutes or 25-35 minutes or in the whole period (0-35 minutes) between the four protocols. No significant differences in central mucus clearance were observed between the four protocols. Comparison ofpatients with emphysema and patients with chronic bronchitis Spontaneous peripheral mucus clearance, as measured in protocol I over 35 minutes, was significantly higher in the patients with Figure 3 Clearance of the radioactive tracer in the patients with chronic bronchitis emphysema than in the patients with chronic from the peripheral lung region in the period 10-20 minutes during thefour different bronchitis (p < 0 005); (fig 4). Central mucus protocols, expressed as a percentage of the starting value (means and standard errors). clearance, however, was similar in the two groups during protocol I. There were no significant differences in peripheral or central mucus clearance between the two groups of patients for the other three protocols. http://thorax.bmj.com/

Discussion Our study showed that spontaneous mucus clearance from the peripheral lung region was greater in patients with decreased than with normal elastic recoil pressure. We observed no significant differences in central mucus clearance between the two groups of patients. We on September 24, 2021 by guest. Protected copyright. tried to match the patients in the two groups .-: ) ( with respect to smoking habit and FEVI % predicted. Although a complete match was not achieved we do not think that this had an important influence on our results; airflow obstruction is likely to have a minor role in spontaneous mucus clearance during tidal breathing. The greater mucus flow from the peripheral region in our patients with emphysema may have masked an increase in central mucus clearance. Camner et al 14 found poorer mucus clearance in patients with chronic bronchitis than in normal subjects, whereas Mossberg et al 5 found normal mucus clearance in patients with emphysema; their patients, however, had no history of hyper- secretion. Spontaneous mucus clearance is probably caused by a combination of mucociliary transport and transport by expiratory airflow. The Figure 4 Clearance of the radioactive tracer in both groups ofpatientsfrom the central area of the surfaces where mucociliary trans- and the peripheral region in the period 0-35 minutes during protocol I, expressed as a port takes place decreases from peripheral to percentage of the starting value (means and standard errors). Bc-bronchitis, clearance from the central region; c--emphysema, clearance from the central region; central airways; the decrease in surface area Be-bronchitis, clearance from the peripheral region; E--emphysema, clearance from may be partly compensated for by a higher the peripheral region. ciliary beat frequency in the central airways.'6 Effect offorced expirations on mucus clearance in patients with chronic airflow obstruction: effect of lung recoil pressure 627 Expiratory airflow during tidal breathing is siderably less in our patients with chronic more effective in clearing mucus when there is airflow obstruction and normal elastic recoil an increased thickness of the mucus layer."7 pressure than in patients with chronic airflow The mucociliary system may be more severely obstruction and decreased elastic recoil pres- affected by the disease process in patients with sure. Forced expirations were less effective in Thorax: first published as 10.1136/thx.45.8.623 on 1 August 1990. Downloaded from chronic bronchitis than in those with treating retention ofmucus in patients with low emphysema, as a result of damaged cilia or than with normal elastic recoil pressure. changes in the rheological characteristics ofthe mucus. We thank Professor Dr H J Sluiter for his critical advice; F Kampen-Bergsma, H C Touw, and W N A Beumkes for their Forced expirations increased peripheral help in preparing the manuscript; D J Buiter for making the mucus transport in the patients with normal or illustrations; and H ter Veen for his assistance in analysing data high elastic recoil pressure but on mucus clearance. This study was supported by a research had little effect grant from the Nederland Astma Fonds. in patients with low elastic recoil pressure, probably because of dynamic bronchial collapse during forced expiration in these 1 Pryor JA, Webber BA. An evaluation of the forced expira- patients. The increase in mucus clearance did tion technique as an adjunct to postural drainage. not correlate with the initial FEV, % predicted Physiotherapy 1979;65:304-7. 2 Pryor JA, Webber BA, Hodson ME, Batten JC. Evaluation (r = 0 03), so the differences in severity of ofthe forced expiration technique as an adjunct to postural airflow obstruction are unlikely to account for drainage in treatment of cystic fibrosis. Br Med J 1979; ii:417-8. our results. 3 Sutton PP, Parker RA, Webber BA, et al. Assessment ofthe Mean mucus clearance was greater during forced expiration technique, postural drainage and direc- ted coughing in chest physiotherapy. Eur J Respir Dis coughing than during forced expirations but 1983;64:62-8. the differences were small and not statistically 4 Verboon JML, Bakker W, Sterk PJ. The value ofthe forced expiration technique with and without postural drainage significant. These results contrast, however, in adults with cystic fibrosis. Eur J Respir Dis 1986; with the patients' assessment, because all 15 69:169-74. 5 Leith DE. Cough. Physical Therapy 1968;48:439-47. thought coughing was the only effective 6 Clarke SW, Jones JG, Oliver DR. Resistance to two-phase method. During coughing the transpulmonary gas-liquidflow in airways. JApplPhysiol 1970;29:464-71. 7 Dawson SV, Elliott EA. Wave-speed limitation on ex- pressure is much higher than during a forced piratory flow-a unifying concept. JApplPhysiol 1977;43: expiration with an open glottis'8 and the energy 498-515. 8 Mead J, Turner JM, Macklem PT, Little JB. Significance of cost is probably higher. Coughing did not, the relationship between lung recoil and maximum however, augment mucus transport when com- expiratory flow. J Appl Physiol 1967;22:95-108. 9 Schans CP van der, Piers DA, Postma DS. Effect ofmanual pared with forced expirations. Forced expira- percussion on tracheobronchial clearance in patients with tions are therefore to be preferred to coughing chronic airflow obstruction and excessive tracheobronchial secretion. Thorax 1986;41:448-52. when additional measures have to be taken to 10 Prato FS, Vinitski S. Radiation dose calculations for inhala- treat mucus retention. tion of Tc-99m sulfur colloid radioaerosol. J Nucl Med 1983;24:816-21. We observed no significant difference be- 11 Simon G, Pride NB, Jones NL, Raimondi AC. Relation tween forced expirations carried out at TLC between abnormalities in the chest radiograph and http://thorax.bmj.com/ changes in pulmonary function in chronic bronchitis and and at FRC. The higher elastic recoil pressure emphysema. Thorax 1973;28:15-23. during forced expiration at TLC does not 12 Cotes JE. Lung function: principles and application in medicine. Oxford: Blackwell, 1979. apparently increase air flow velocity suf- 13 Nie NH. SPSSstatisticalpackagefor the socialsciences second ficiently to increase mucus transport to a edition. New York: McGraw-Hill, 1975. 14 Camner P, Mossberg B, Philipson K. Tracheobronchial greater extent than a forced expiration at FRC. clearance and chronic obstructive lung disease. Scand J Several authors have suggested that physio- Respir Dis 1973;54:272-81. 15 Mossberg B, Philipson K, Camner P. Tracheobronchial therapy is effective only when the mucus clearance in patients with emphysema associated with expectoration is more than 30 ml a day.'9 Our alpha l-antitrypsin deficiency. Scand J Respir Dis 1978; on September 24, 2021 by guest. Protected copyright. 59:1-7. study has shown that both forced expirations 16 Rutland J, Griffin WM, Cole PJ. Human ciliary beat and coughing are also effective in patients who frequency in epithelium from intrathoracic and extra- thoracic airways. Am Rev Respir Dis 1982;125:100-5. expectorate less. Expectoration of mucus may 17 Kim CS, Rodriguez CR, Eldridge MA, Sackner MA. not lead to an improvement of lung function Criteria for mucus transport in the airways by two-phase gas-liquid flow mechanism. JApplPhysiol 1986;60:901-7. but it may contribute to the prevention of 18 Langlands J. The dynamics ofcough in health and in chronic pulmonary infections. bronchitis. Thorax 1967;22:88-96. 19 KiriloffLH, Owens GR, Rogers RM, Mazzocco MG. Does In conclusion, mucus clearance was con- chest physical therapy work? Chest 1985;88:436-44.